Downloaded from rsbl.royalsocietypublishing.org on February 22, 2011 Female bonobos use copulation calls as social signals Zanna Clay, Simone Pika, Thibaud Gruber and Klaus Zuberbühler Biol. Lett. published online 16 February 2011 doi: 10.1098/rsbl.2010.1227 Supplementary data "Data Supplement" http://rsbl.royalsocietypublishing.org/content/suppl/2011/02/15/rsbl.2010.1227.DC1.ht ml References This article cites 16 articles, 4 of which can be accessed free http://rsbl.royalsocietypublishing.org/content/early/2011/02/15/rsbl.2010.1227.full.html #ref-list-1 P<P Published online 16 February 2011 in advance of the print journal. Subject collections Articles on similar topics can be found in the following collections behaviour (1818 articles) cognition (456 articles) Receive free email alerts when new articles cite this article - sign up in the box at the top Email alerting service right-hand corner of the article or click here Advance online articles have been peer reviewed and accepted for publication but have not yet appeared in the paper journal (edited, typeset versions may be posted when available prior to final publication). Advance online articles are citable and establish publication priority; they are indexed by PubMed from initial publication. Citations to Advance online articles must include the digital object identifier (DOIs) and date of initial publication. To subscribe to Biol. Lett. go to: http://rsbl.royalsocietypublishing.org/subscriptions This journal is © 2011 The Royal Society Downloaded from rsbl.royalsocietypublishing.org on February 22, 2011 Biol. Lett. cognitive processes underlying call production. In doi:10.1098/rsbl.2010.1227 Barbary macaques (Macaca sylvanus), for example, Published online females can elicit and time the onset of male ejacula- Animal behaviour tion using copulation calls [7]. In chimpanzees (Pan troglodytes), females advertise matings with high- ranked males but inhibit calling in the presence of Female bonobos use higher ranked female audiences, possibly as a means to reduce female competition [8]. copulation calls as Female bonobos (Pan paniscus) produce copulation calls during mating events [9].Foranumberofreasons, social signals this primate represents an intriguing species to study Zanna Clay, Simone Pika, Thibaud Gruber copulation calls. Females are the principally emigrating and Klaus Zuberbu¨ hler* sex [10,11] but, despite the absence of kinship ties, they are highly gregarious and form strong bonds with School of Psychology, University of St Andrews, St Andrews KY16 9JP, UK one another [9,11]. Related to this is a heightened sexu- *Author for correspondence ([email protected]). ality, frequently divorced from reproduction, with females commonly engaging in sexual interactions in all During mating events, females of many primate species produce loud and distinct vocalizations age and sex combinations [9,12,13]. Sex appears to known as ‘copulation calls’. The adaptive signifi- also serve as a social tool, facilitating the integration of cance of these signals is considered to be in young females into their new community and their promoting the caller’s direct reproductive suc- subsequently peaceful coexistence and affiliation with cess. Here, we investigated copulation calling in non-related group members (e.g. [9,11–13]). bonobos (Pan paniscus), a species in which Sexual interactions between bonobo females are females produce these vocalizations during known as ‘genital contacts’, whereby individuals sexual interactions with partners of both sexes. embrace ventro-ventrally and swing their hips laterally, Females were more likely to call when mating while keeping their vulvae in contact [12,13]. Intrigu- with males than with females. We also observed ingly, females sometimes produce vocalizations during a positive relationship between the likelihood of calling and partner rank, regardless of partner these events [9]. We term them copulation calls follow- sex. Sexual activity generally increased with ing recent acoustic analyses showing that these calls swelling size (an indicator of reproductive state) cannot be distinguished from those produced when and, during their peak swelling, females called mating with males [14]. The production of copulation more with male than with female partners. calls during homosexual interactions is not well Female bonobos are unusual among the non- explained by existing theories of primate copulation human primates in terms of their heightened calls, which all focus on reproductive significance. socio-sexuality. Our results suggest that in this Theaimofthepresentstudywastoexaminethefunc- species, copulation calls have undergone an evol- tion and usage of copulation calls in female bonobos by utionary transition from a purely reproductive to focusing especially on both homo- and heterosexual a more general social function, reflecting the encounters and partner rank. We also examined whether intrinsic evolutionary links between vocal behaviour and social cognition. a physical variable associated with reproductive state, sexual swelling size, influenced call production. Our Keywords: primate vocalization; sexual selection; general prediction was that, if copulation calls were social intelligence used as a social rather than an exclusively reproductive signal, similar patterns of call production with both male and female partners should be found. 1. INTRODUCTION Females of many primate species produce loud and 2. MATERIAL AND METHODS distinct vocalizations during mating events. These sig- We conducted observations of three bonobo groups at Lola Ya nals, known as ‘copulation calls’ [1], are especially Bonobo Sanctuary, Kinshasa, DR Congo, between September and widespread among Old World species in which the November 2008 and between August and November 2009. The females are promiscuous, live in multi-male multi- daily routine at the sanctuary remained the same throughout obser- vation periods (electronic supplementary material). In 2008, we female groups and advertise their receptivity with observed individuals in one of the two largest enclosures, henceforth sexual swellings [2]. While many functional hypotheses ‘group 1a’. In 2009, we collected data from two groups housed in the have been put forward, all essentially converge on the same and the adjacent enclosure, henceforth ‘group 1b’ and unifying notion that copulation calls are part of sexu- ‘group 2’. Group composition in the first enclosure changed between the two study periods (group 1a: n ¼ 9 females, n ¼ 9 ally selected strategies that promote the reproductive males, n ¼ 4 infants; group 1b: n ¼ 7 females, n ¼ 9males,n ¼ 4 success of the caller [1,3]. For example, calls may infants; group 2: n ¼ 5 females, n ¼ 11 males; n ¼ 3infants; attract mates and signal female receptivity, in turn electronic supplementary material, table S1). We pooled the data across the three groups and combined data for dyads that met inciting male–male competition directly [4] or via again in the second year (n ¼ 9 female–female dyads; n ¼ 19 sperm competition [5]. Alternatively, calls may male–female dyads). reduce risks of infanticide by promoting paternity In bonobos, sexual behaviour can take a variety of forms, such as uncertainty or enhancing mate guarding [6]. There is heterosexual copulations (with pelvic thrusts and intromission), mountings, homosexual genital contacts and genital stimulation also some evidence of strategic call use, suggesting using an object or body part. Here, we recorded behaviours and that copulation calls can provide a window into the vocalizations of females engaging in copulations with males or genital contacts with females. Copulation calls were acoustically distinct and Electronic supplementary material is available at http://dx.doi.org/ never observed in contexts other than sexual interactions. We con- 10.1098/rsbl.2010.1227 or via http://rsbl.royalsocietypublishing.org. ducted observations using all-day focal and ad libitum sampling Received 24 December 2010 Accepted 1 February 2011 This journal is q 2011 The Royal Society Downloaded from rsbl.royalsocietypublishing.org on February 22, 2011 2 Z. Clay et al. Bonobo copulation calls methods (approx. n ¼ 1093 h), balanced across individuals. We recorded female vocalizations at distances of 3–20 m using a 100 Sennheiser MKH816T directional microphone and Marantz PMD660 solid-state recorder (sampling rate of 44.1 kHz, 16 bits accuracy). Bonobo copulation calls typically consist of a single or succession of high-frequency squeaks and screams that usually 80 begin during the copulation [9] (electronic supplementary material, figure S1). We also recorded female reproductive states following veterinary assessments and collected daily records of swelling sizes, using Furuichi’s [15] 4-point scale based on degree of wrinkling. 60 To assess the influence of dominance, we used hierarchies calcu- lated for another study on the same study groups and period [14], based on the outcome of dyadic agonistic interactions. We used ‘flee- ing upon aggression’ as a behavioural marker for subordinance [16]. 40 Dominance relationships and linearity were calculated with the Matman matrix analysis program (NOLDUS v. 1.1). We calculated and tested the adjusted linearity index h0, corrected for unknown relationships [16–18], as well as the directional consistency index interactions with call % sexual 20 (electronic supplementary material, table S2). For significantly linear hierarchies, we calculated individual cardinal ranks, using normalized David’s scores